Long-Term Overconsumption of Fat and Sugar Causes a Partially Reversible Pre-inflammatory Bowel Disease State

Nutrition appears to be an important environmental factor involved in the onset of inflammatory bowel diseases (IBD) through yet poorly understood biological mechanisms. Most studies focused on fat content in high caloric diets, while refined sugars represent up to 40% of caloric intake within indus...

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Autores principales: Djésia Arnone, Marie Vallier, Sébastien Hergalant, Caroline Chabot, Ndeye Coumba Ndiaye, David Moulin, Anda-Maria Aignatoaei, Jean-Marc Alberto, Huguette Louis, Olivier Boulard, Camille Mayeur, Natacha Dreumont, Kenneth Peuker, Anne Strigli, Sebastian Zeissig, Franck Hansmannel, Matthias Chamaillard, Tunay Kökten, Laurent Peyrin-Biroulet
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Publicado: Frontiers Media S.A. 2021
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Acceso en línea:https://doaj.org/article/2ee22f86cf98438b86870d25a1c9fca1
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spelling oai:doaj.org-article:2ee22f86cf98438b86870d25a1c9fca12021-11-18T09:19:44ZLong-Term Overconsumption of Fat and Sugar Causes a Partially Reversible Pre-inflammatory Bowel Disease State2296-861X10.3389/fnut.2021.758518https://doaj.org/article/2ee22f86cf98438b86870d25a1c9fca12021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fnut.2021.758518/fullhttps://doaj.org/toc/2296-861XNutrition appears to be an important environmental factor involved in the onset of inflammatory bowel diseases (IBD) through yet poorly understood biological mechanisms. Most studies focused on fat content in high caloric diets, while refined sugars represent up to 40% of caloric intake within industrialized countries and contribute to the growing epidemics of inflammatory diseases. Herein we aim to better understand the impact of a high-fat-high-sucrose diet on intestinal homeostasis in healthy conditions and the subsequent colitis risk. We investigated the early events and the potential reversibility of high caloric diet-induced damage in mice before experimental colitis. C57BL/6 mice were fed with a high-fat or high-fat high-sucrose or control diet before experimental colitis. In healthy mice, a high-fat high-sucrose diet induces a pre-IBD state characterized by gut microbiota dysbiosis with a total depletion of bacteria belonging to Barnesiella that is associated with subclinical endoscopic lesions. An overall down-regulation of the colonic transcriptome converged with broadly decreased immune cell populations in the mesenteric lymph nodes leading to the inability to respond to tissue injury. Such in-vivo effects on microbiome and transcriptome were partially restored when returning to normal chow. Long-term consumption of diet enriched in sucrose and fat predisposes mice to colitis. This enhanced risk is preceded by gut microbiota dysbiosis and transcriptional reprogramming of colonic genes related to IBD. Importantly, diet-induced transcriptome and microbiome disturbances are partially reversible after switching back to normal chow with persistent sequelae that may contribute to IBD predisposition in the general population.Djésia ArnoneMarie VallierSébastien HergalantCaroline ChabotNdeye Coumba NdiayeDavid MoulinAnda-Maria AignatoaeiJean-Marc AlbertoHuguette LouisHuguette LouisOlivier BoulardCamille MayeurNatacha DreumontKenneth PeukerKenneth PeukerAnne StrigliAnne StrigliSebastian ZeissigSebastian ZeissigFranck HansmannelMatthias ChamaillardTunay KöktenLaurent Peyrin-BirouletLaurent Peyrin-BirouletFrontiers Media S.A.articlediet-inducedIBD-inflammatory bowel diseasescolitisgut homeostasishigh-fat high-sucrose dietNutrition. Foods and food supplyTX341-641ENFrontiers in Nutrition, Vol 8 (2021)
institution DOAJ
collection DOAJ
language EN
topic diet-induced
IBD-inflammatory bowel diseases
colitis
gut homeostasis
high-fat high-sucrose diet
Nutrition. Foods and food supply
TX341-641
spellingShingle diet-induced
IBD-inflammatory bowel diseases
colitis
gut homeostasis
high-fat high-sucrose diet
Nutrition. Foods and food supply
TX341-641
Djésia Arnone
Marie Vallier
Sébastien Hergalant
Caroline Chabot
Ndeye Coumba Ndiaye
David Moulin
Anda-Maria Aignatoaei
Jean-Marc Alberto
Huguette Louis
Huguette Louis
Olivier Boulard
Camille Mayeur
Natacha Dreumont
Kenneth Peuker
Kenneth Peuker
Anne Strigli
Anne Strigli
Sebastian Zeissig
Sebastian Zeissig
Franck Hansmannel
Matthias Chamaillard
Tunay Kökten
Laurent Peyrin-Biroulet
Laurent Peyrin-Biroulet
Long-Term Overconsumption of Fat and Sugar Causes a Partially Reversible Pre-inflammatory Bowel Disease State
description Nutrition appears to be an important environmental factor involved in the onset of inflammatory bowel diseases (IBD) through yet poorly understood biological mechanisms. Most studies focused on fat content in high caloric diets, while refined sugars represent up to 40% of caloric intake within industrialized countries and contribute to the growing epidemics of inflammatory diseases. Herein we aim to better understand the impact of a high-fat-high-sucrose diet on intestinal homeostasis in healthy conditions and the subsequent colitis risk. We investigated the early events and the potential reversibility of high caloric diet-induced damage in mice before experimental colitis. C57BL/6 mice were fed with a high-fat or high-fat high-sucrose or control diet before experimental colitis. In healthy mice, a high-fat high-sucrose diet induces a pre-IBD state characterized by gut microbiota dysbiosis with a total depletion of bacteria belonging to Barnesiella that is associated with subclinical endoscopic lesions. An overall down-regulation of the colonic transcriptome converged with broadly decreased immune cell populations in the mesenteric lymph nodes leading to the inability to respond to tissue injury. Such in-vivo effects on microbiome and transcriptome were partially restored when returning to normal chow. Long-term consumption of diet enriched in sucrose and fat predisposes mice to colitis. This enhanced risk is preceded by gut microbiota dysbiosis and transcriptional reprogramming of colonic genes related to IBD. Importantly, diet-induced transcriptome and microbiome disturbances are partially reversible after switching back to normal chow with persistent sequelae that may contribute to IBD predisposition in the general population.
format article
author Djésia Arnone
Marie Vallier
Sébastien Hergalant
Caroline Chabot
Ndeye Coumba Ndiaye
David Moulin
Anda-Maria Aignatoaei
Jean-Marc Alberto
Huguette Louis
Huguette Louis
Olivier Boulard
Camille Mayeur
Natacha Dreumont
Kenneth Peuker
Kenneth Peuker
Anne Strigli
Anne Strigli
Sebastian Zeissig
Sebastian Zeissig
Franck Hansmannel
Matthias Chamaillard
Tunay Kökten
Laurent Peyrin-Biroulet
Laurent Peyrin-Biroulet
author_facet Djésia Arnone
Marie Vallier
Sébastien Hergalant
Caroline Chabot
Ndeye Coumba Ndiaye
David Moulin
Anda-Maria Aignatoaei
Jean-Marc Alberto
Huguette Louis
Huguette Louis
Olivier Boulard
Camille Mayeur
Natacha Dreumont
Kenneth Peuker
Kenneth Peuker
Anne Strigli
Anne Strigli
Sebastian Zeissig
Sebastian Zeissig
Franck Hansmannel
Matthias Chamaillard
Tunay Kökten
Laurent Peyrin-Biroulet
Laurent Peyrin-Biroulet
author_sort Djésia Arnone
title Long-Term Overconsumption of Fat and Sugar Causes a Partially Reversible Pre-inflammatory Bowel Disease State
title_short Long-Term Overconsumption of Fat and Sugar Causes a Partially Reversible Pre-inflammatory Bowel Disease State
title_full Long-Term Overconsumption of Fat and Sugar Causes a Partially Reversible Pre-inflammatory Bowel Disease State
title_fullStr Long-Term Overconsumption of Fat and Sugar Causes a Partially Reversible Pre-inflammatory Bowel Disease State
title_full_unstemmed Long-Term Overconsumption of Fat and Sugar Causes a Partially Reversible Pre-inflammatory Bowel Disease State
title_sort long-term overconsumption of fat and sugar causes a partially reversible pre-inflammatory bowel disease state
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/2ee22f86cf98438b86870d25a1c9fca1
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